Ancient DNA analysis reveals high frequency of european lactase persistence allele (T-13910) in medieval Central Europe

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Krüttli, Annina ^a   Bouwman, Abigail ^a   Akgül, Gülfirde ^a   Casa, Philippe Della ^a   Rühli, Frank ^a   Warinner, Christina ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; LACTASE; MITOCHONDRIAL DNA; THYMINE;

ARTICLE; AUSTRIA; CONTROLLED STUDY; DNA DETERMINATION; DNA EXTRACTION; DNA SEQUENCE; ETHNIC GROUP; EUROPEAN; FEMALE; GENE FREQUENCY; GENETIC TRAIT; GENOTYPE; GERMANY; HUMAN; MALE; MIDDLE AGES; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NEOLITHIC; POPULATION GENETICS; POPULATION RESEARCH; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ANIMALS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FEMALE; GENE FREQUENCY; GERMANY; HISTORY, MEDIEVAL; HUMANS; LACTASE; LACTOSE INTOLERANCE; MALE; MILK; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA;

EID: 84899817472     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086251     Document Type: Article

References (50)

1. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, et al. (2002) Identification of a variant associated with adult-type hypolactasia. Nat Genet 30: 233-237.
2. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, et al. (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31-40. (Pubitemid 46026499)
3. Enattah NS, Jensen TGK, Nielsen M, Lewinski R, Kuokkanen M, et al. (2008) Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am J Hum Genet 82: 57-72. (Pubitemid 351735951)
4. Ingram CJ, Elamin MF, Mulcare CA, Weale ME, Tarekegn A, et al. (2007) A novel polymorphism associated with lactose tolerance in Africa: multiple causes for lactase persistence? Human Genetics 120: 779-788. (Pubitemid 46128833)
5. Durham WH (1991) Cultural mediation: the evolution of adult lactose absorption. In: Durham WH, editor. Coevolution : genes, culture, and human diversity. Stanford, Calif.: Stanford University Press. pp. 226-285.
6. Itan Y, Jones BL, Ingram CJ, Swallow DM, Thomas MG (2010) A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol 10: 36.
7. Bodlaj G, Stocher M, Hufnagl P, Hubmann R, Biesenbach G, et al. (2006) Genotyping of the lactase-phlorizin hydrolase -13910 polymorphism by LightCycler PCR and implications for the diagnosis of lactose intolerance. Clin Chem 52: 148-151. (Pubitemid 43032480)
8. Buning C, Ockenga J, Kruger S, Jurga J, Baier P, et al. (2003) The C/C(-13910) and G/G(-22018) genotypes for adult-type hypolactasia are not associated with inflammatory bowel disease. Scand J Gastroenterol 38: 538-542. (Pubitemid 36609861)
9. Clar H, Renner W, Krippl P, Leithner A, Gruber G, et al. (2008) The LCT 13910 C/T polymorphism as a risk factor for osteoporosis, has no impact on metastatic bone disease in breast cancer. Breast Cancer Res Treat 112: 363-365.
10. Obermayer-Pietsch BM, Bonelli CM, Walter DE, Kuhn RJ, Fahrleitner-Pammer A, et al. (2004) Genetic predisposition for adult lactose intolerance and relation to diet, bone density, and bone fractures. J Bone Miner Res 19: 42-47. (Pubitemid 41295136)
11. Tag CG, Oberkanins C, Kriegshauser G, Ingram CJ, Swallow DM, et al. (2008) Evaluation of a novel reverse-hybridization StripAssay for typing DNA variants useful in diagnosis of adult-type hypolactasia. Clin Chim Acta 392: 58-62.
12. Beja-Pereira A, Luikart G, England PR, Bradley DG, Jann OC, et al. (2003) Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat Genet 35: 311-313. (Pubitemid 37486911)
13. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, et al. (2004) Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74: 1111-1120. (Pubitemid 38669310)
14. Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG (2007) Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc Natl Acad Sci U S A 104: 3736-3741. (Pubitemid 47181524)
15. Enattah NS, Jensen TG, Nielsen M, Lewinski R, Kuokkanen M, et al. (2008) Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am J Hum Genet 82: 57-72. (Pubitemid 351735951)
16. Evershed RP, Payne S, Sherratt AG, Copley MS, Coolidge J, et al. (2008) Earliest date for milk use in the Near East and southeastern Europe linked to cattle herding. Nature 455: 528-531.
17. Gerbault P, Liebert A, Itan Y, Powell A, Currat M, et al. (2011) Evolution of lactase persistence: an example of human niche construction. Philos Trans R Soc Lond B Biol Sci 366: 863-877.
18. Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG (2009) The Origins of Lactase Persistence in Europe. PLoS Comput Biol 5.
19. Jakobsson M, Scholz SW, Scheet P, Gibbs JR, VanLiere JM, et al. (2008) Genotype, haplotype and copy-number variation in worldwide human populations. Nature 451: 998-1003. (Pubitemid 351301742)
20. Nielsen R, Hellmann I, Hubisz M, Bustamante C, Clark AG (2007) Recent and ongoing selection in the human genome. Nat Rev Genet 8: 857-868. (Pubitemid 47609088)
21. Omenn GS (2010) Evolution in health and medicine Sackler colloquium: Evolution and public health. Proc Natl Acad Sci U S A 107 Suppl 1: 1702-1709.
22. Schlebusch CM, Sjodin P, Skoglund P, Jakobsson M (2013) Stronger signal of recent selection for lactase persistence in Maasai than in Europeans. European Journal of Human Genetics 21: 550-553.
23. Vigne J-D, Helmer D (2007) Was milk a "secondary product" in the Old World Neolithisation process? Its role in the domestication of cattle, sheep and goats. Anthropozoologica 42: 9-40.
24. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.
25. Mccracke.Rd (1971) Lactase Deficiency - Example of Dietary Evolution. Current Anthropology 12: 479-&.
26. Nei M, Saitou N (1986) Genetic relationship of human populations and ethnic differences in reaction to drugs and food. Prog Clin Biol Res 214: 21-37.
27. Cook GC, Altorki MT (1975) High Intestinal Lactase Concentrations in Adult Arabs in Saudi-Arabia. British Medical Journal 3: 135-136.
28. Flatz G, Rotthauwe HW (1973) Lactose nutrition and natural selection. Lancet 2: 76-77.
29. Konje JC, Ladipo OA (2000) Nutrition and obstructed labor. Am J Clin Nutr 72: 291S-297S. (Pubitemid 30439801)
30. Lee VA, Lorenz K (1978) The nutritional and physiological impact of milk in human nutrition. CRC Crit Rev Food Sci Nutr 11: 41-116.
31. Benecke N (1994) Der Mensch und seine Haustiere: die Geschichte einer jahrtausendealten Beziehung: Theiss Stuttgart.
32. Balasse M, Tresset A (2002) Early weaning of Neolithic domestic cattle (Bercy, France) revealed by intra-tooth variation in nitrogen isotope ratios. Journal of Archaeological Science 29: 853-859. (Pubitemid 34949626)
33. Coelho M, Luiselli D, Bertorelle G, Lopes AI, Seixas S, et al. (2005) Microsatellite variation and evolution of human lactase persistence. Human Genetics 117: 329-339. (Pubitemid 41194559)
34. Plantinga TS, Alonso S, Izagirre N, Hervella M, Fregel R, et al. (2012) Low prevalence of lactase persistence in Neolithic South-West Europe (vol 20, pg 778, 2012). European Journal of Human Genetics 20: 810-810.
35. Malmstrom H, Linderholm A, Liden K, Stora J, Molnar P, et al. (2010) High frequency of lactose intolerance in a prehistoric hunter-gatherer population in northern Europe. BMC Evol Biol 10.
36. Lacan M, Keyser C, Ricaut FX, Brucato N, Duranthon F, et al. (2011) Ancient DNA reveals male diffusion through the Neolithic Mediterranean route. Proc Natl Acad Sci U S A 108: 9788-9791.
37. Lacan M, Keyser C, Ricaut FX, Brucato N, Tarrus J, et al. (2011) Ancient DNA suggests the leading role played by men in the Neolithic dissemination. Proc Natl Acad Sci U S A 108: 18255-18259.
38. Nagy D, Tomory G, Csanyi B, Bogacsi-Szabo E, Czibula A, et al. (2011) Comparison of Lactase Persistence Polymorphism in Ancient and Present-Day Hungarian Populations. American Journal of Physical Anthropology 145: 262-269.
39. Hofmann MI, Böni T, Alt KW, Woitek U, Rühli FJ (2008) Paleopathologies of the vertebral column in medieval skeletons. Anthropologischer Anzeiger 66: 1-17.
40. Galvani AP, Novembre J (2005) The evolutionary history of the CCR5-Delta32 HIV-resistance mutation. Microbes Infect 7: 302-309.
41. Stephens JC, Reich DE, Goldstein DB, Shin HD, Smith MW, et al. (1998) Dating the origin of the CCR5-Delta32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62: 1507-1515. (Pubitemid 28307122)
42. Pieper R (2003) Kloster Dalheim: Eine kurze Geschichte. Münster: Land-schaftsverband Westfalen-Lippe.
43. Champlot S, Berthelot C, Pruvost M, Bennett EA, Grange T, et al. (2010) An Efficient Multistrategy DNA Decontamination Procedure of PCR Reagents for Hypersensitive PCR Applications. PLoS One 5.
44. Gilbert MT, Bandelt HJ, Hofreiter M, Barnes I (2005) Assessing ancient DNA studies. Trends in Ecology & Evolution 20: 541-544. (Pubitemid 41323710)
45. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23: 147. (Pubitemid 29455385)
46. Alonso A, Martin P, Albarran C, Garcia P, Garcia O, et al. (2004) Real-time PCR designs to estimate nuclear and mitochondrial DNA copy number in forensic and ancient DNA studies. Forensic Sci Int 139: 141-149. (Pubitemid 38201113)
47. Ginolhac A, Rasmussen M, Gilbert MTP, Willerslev E, Orlando L (2011) mapDamage: testing for damage patterns in ancient DNA sequences. Bioinformatics 27: 2153-2155.
48. Willerslev E, Cooper A (2005) Ancient DNA. Proc Biol Sci 272: 3-16.
49. Malmstrom H, Svensson EM, Gilbert MT, Willerslev E, Gotherstrom A, et al. (2007) More on contamination: the use of asymmetric molecular behavior to identify authentic ancient human DNA. Mol Biol Evol 24: 998-1004. (Pubitemid 46536708)
50. Team RC (2013) R: A language and environment for statistical computing. 3.0.1 (2013-05-16) ed. Vienna, Austria: R Foundation for Statistical Computing.